A systematic review: endometriosis presenting with ascites

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Arch Gynecol Obstet (2011) 283:513–518 DOI 10.1007/s00404-010-1664-1


A systematic review: endometriosis presenting with ascites Tayfun Gungor • Mine Kanat-Pektas • Mustafa Ozat • Mujdegul Zayifoglu Karaca

Received: 6 May 2010 / Accepted: 24 August 2010 / Published online: 7 September 2010 Ó Springer-Verlag 2010

Abstract Background The present review aims to increase the awareness of the gynecologists by analyzing all the case reports which refer to endometriosis presenting either with only ascites or with massive ascites with pleural effusion. Methods To conduct the present review, the CENTRAL (in the Cochrane Library, current issue), MEDLINE (Silver Platter, from 1950 to 2010), and EMBASE (from 1950 to 2010) electronic databases were searched. As a result, all the publications based on the keywords relating to the review topic were acquired. Results Since the description of first case in 1954, endometriosis-related ascites was reported to occur in a total of 63 women who were aged between 19 and 51 years. Approximately 63.0% of the recruited women for whom ethnicity was specified were of African origin (29 out of 46). Of the 50 subjects with known obstetric history, 41 (82.0%) were nulliparous. Abdominal distention, anorexia/weight loss, abdominal pain, and menometrorrhagia were the most frequently encountered clinical symptoms, whereas pelvic mass was the most common physical finding. The serum concentrations of CA 125 were between 20 and 3,504 IU/ml for 19 women whose CA 125 levels were determined. Pleural effusion was also present in 38.1% of the reviewed subjects (24 out of 63). The clinical features of the women with endometriosis-related T. Gungor  M. Ozat  M. Zayifoglu Karaca Department of Gynecology, Dr. Zekai Tahir Burak Women Health Research and Education Hospital, Ankara, Turkey M. Kanat-Pektas (&) Department of Obstetrics and Gynecology, Etlik Ihtisas Research and Education Hospital, Yunus Emre Mah, Dereboyu Sok. No: 71/2 Yenimahalle, 06170 Ankara, Turkey e-mail: [email protected]

ascites and pleural effusion were similar to those of the women who had only endometriosis-related ascites. Conclusion Endometriosis-related ascites and/or pleural effusion refers to extensive disease with a high risk for recurrence which usually affects non-Caucasian, nulliparous women of reproductive age and leads to clinical symptoms resembling those of an ovarian malignancy. Therefore, clinicians should consider endometriosis in differential diagnosis of pelvic masses and also include endometriosis in diagnostic workup of ascites or pleural effusion. Keywords

Ascites  Endometriosis  Pleural effusion

Introduction The term ascites refers to the pathological accumulation of fluid within the peritoneal cavity. Ascites usually develops due to liver disease, congestive cardiac failure, or nephrotic syndrome. Certain gynecological diseases, such as ovarian tumors, pelvic or peritoneal tuberculosis, ovarian hyperstimulation syndrome, and Meigs syndrome can cause ascites as well. Amongst all gynecological diseases resulting in ascites, endometriosis is uncommonly encountered [1]. Endometriosis is a relatively common disease which is estimated to have a prevalence of up to 10% among the general population. Endometriosis is detected in 30% of women undergoing evaluation for infertility and 30–40% of women with dysmenorrhea and pelvic pain. This unique pathology is defined by the ectopic presence of endometrial epithelium and stroma outside the uterine cavity. Endometriosis frequently presents with pelvic pain, pelvic tenderness, dysmenorrhea, dyspareunia, and a history of infertility [2–4].



Most of the gynecologists are unaware that endometriosis may present with ascites and even pleural effusion as well. That is why endometriosis-related ascites is commonly mistaken for ascites associated with an ovarian neoplasm. Sometimes the existence of symptoms, such as weight loss or poor appetite and the visualization of a pelvic mass may further complicate the situation. Another condition contributing to the diagnostic dilemma is the elevation in the serum levels of tumor markers which are commonly used in the evaluation of ovarian masses so that the diagnosis of ovarian malignancy almost appears to be certain [5–7]. The unusual co-occurrence of endometriosis and ascites is rarely encountered, with 57 publications made ever since the first case report was represented in 1954 [8–64]. The present review aims to determine the demographic and clinical features of women presenting with endometriosisassociated ascites and/or pleural effusion by analyzing all the published case reports.

Materials and methods To conduct the present review, two of the investigators (M.K.P. and T.G.) searched the following electronic databases for the registered case reports: CENTRAL (in the Cochrane Library, current issue), MEDLINE (Silver Platter, from 1954 to 2010), and EMBASE (from 1954 to 2010). As for all of the electronic databases, a search strategy was developed so that all of the publications based on the keywords relating to the review topic could be acquired. These key terms were identified as ‘‘endometriosis’’, ‘‘massive ascites’’, and ‘‘pleural effusion’’. After that, all free text MH exact subject headings (MeSH) and MeSH terms were explored. Any new terms found were fed into the search strategy so that new searches could be run. Consequently the relevant articles were identified and scanned. The reference lists of the relevant papers that were available were scrutinized for further studies. Besides relevant articles were re-entered into PubMed (up to July 2010), and by using the ‘‘related articles’’ feature, a further search was carried out. The inclusion criteria were all publications (including case reports, short communications, and letters to the editor) which refer to endometriosis presenting with ascites or ascites and pleural effusion. The exclusion criteria included all of the duplicate publications and unavailability to reach the full text of the article. In case a duplicate publication is detected, the most recent study was included. Since there was no language restriction, the papers in all languages were sought and translated. On the other hand, there was inconvenience to reach the full text in four of the retrieved publications. Therefore, contact with the corresponding


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authors was attempted by means of electronic mail to which two of the corresponding authors responded. After the recruited papers were independently investigated by two of the investigators (M.K.P. and T.G.), the required data were extracted and recorded in computerized media by the remaining investigator (M.O.). Collected data were recorded and descriptive statistics were analyzed by means of Statistical Package for Social Sciences version 11.5 (SPSS Inc., Chicago, IL, USA). Continuous variables were expressed as minimum-tomaximum range or percentage where appropriate.

Results The search in the existing electronic databases has led to the identification of 57 scientific articles which described women who were diagnosed with endometriosis-associated ascites and/or pleural effusion. However, the researchers were able to reach the full text paper in 55 out of 57 retrieved articles (96.5%). Thus, the remaining two articles were excluded. No duplicate publications were detected. According to the present investigation, endometriosisrelated ascites was reported to occur in a total of 63 women since the description of first case in 1954. The age of these women was found to be between 19 and 51 years. The ethnicity was unspecified in 22.2% of the reviewed subjects (14 out of 63). Nevertheless, 63.0% of the recruited women for whom ethnicity was specified were of African origin (29 out of 46). The obstetric history was undetermined in 13 subjects (20.6%) which had been claimed to have endometriosis-related ascites. Of the remaining patients, 82.0% (41 out of 50) were nulliparous. One of the women with endometriosis-related ascites was reported to have Turner syndrome [24], while the other one with cyclic ascites suffered from familial Mediterranean fever [22]. Meanwhile, a case report by Haeri et al. [60] defined a woman with acquired immunodeficiency syndrome in whom endometriosis-associated ascites appeared. Another interesting case report described a young woman who underwent hypovolemic shock due to endometriosisrelated ascites [63]. Table 1 demonstrates the clinical symptoms and physical findings which were associated with ascites and pleural effusion caused by endometriosis. Thus, abdominal distention, anorexia/weight loss, abdominal pain, and menometrorrhagia were the most frequent clinical symptoms. As for the physical findings, pelvic mass was detected most commonly. The serum concentrations of CA 125 were between 20 and 3,504 IU/ml for 19 women in whom endometriosis-associated ascites was diagnosed and CA 125 level was determined. Ovarian malignancy was suspected during the diagnostic workout of 33 cases (52.4%).

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Table 1 Clinical symptoms and physical findings in the reviewed subjects

Table 2 Medical and surgical management of the reviewed cases Number (%)

Number (%) Medical management Clinical symptoms

Gonadotropin releasing hormone agonist

29 (46.0)

Abdominal distention

45 (71.4)


11 (17.5)

Anorexia/Weight loss

38 (60.3)


9 (14.3)

Abdominal pain

33 (52.4)

Danazol ? Progesterone

7 (11.1)


22 (34.9)

Oral contraceptives

5 (7.9)


12 (19.1)


2 (3.2)

Nausea/Emesis Abdominal discomfort

10 (15.9) 7 (11.1)

Surgical management Laparotomy (excision of adnexal mass)

23 (36.5)


5 (7.9)


14 (22.2)


4 (6.3)

Pelvic pain

4 (6.3)

Ovarian wedge biopsy Unilateral salpingo-oopherectomy

Change in bowel habits

3 (4.8)

Only adhesiolysis

3 (4.8)

Chest pain

1 (1.6)


2 (3.2)

Physical findings Pelvic mass

21 (35.0)

Pelvic nodularity

12 (20.0)

Adnexal mass

11 (18.3)

Diminished breath sounds

3 (3.3)

Physical findings due to hypovolemiaa

1 (1.7)


Physical findings due to hypovolemia include tachycardia, hypotension, and turgor loss

Table 2 displays the medical and surgical treatment methods that had been adopted for the management of the reviewed patients. In 10 out of 63 patients (15.9%), there were adhesions associated with advanced stage endometriosis so adhesiolysis was performed. Pleural effusion was also present in 38.1% of the reviewed subjects who had endometriosis-related ascites (24 out of 63). The age of these women differed between 21 and 51 years. More than half of the patients with endometriosis-associated pleural effusion were of African origin (54.2%, 13 out of 24) and the majority of these patients were nulliparous (66.7%, 16 out of 24). The most frequently observed clinical symptoms were abdominal distention (83.3%, 20 out of 24), anorexia/weight loss (62.5%, 15 out of 24), and abdominal pain (45.8%, 11 out of 24), respectively. Besides pelvic adhesions were detected in five patients with endometriosis-related pleural effusion (20.8%). The serum concentrations of CA 125 were between 20 and 3,504 IU/ml for 10 women with endometriosis-associated ascites for whom CA 125 level was determined.

Discussion Endometriosis generally involves the peritoneum, ovaries, and rectovaginal septum. Therefore, the most frequently

8 (12.7) 5 (7.9)

Bilateral salpingo-oopherectomy

1 (1.6)

No surgical treatment

7 (11.1)


63 (100.0)

observed symptoms of endometriosis include dysmenorrhea, pelvic pain, deep dyspareunia, and infertility. Endometriosis may also involve the gastrointestinal tract, urinary tract, or extra abdominal sites, giving rise to a wide variety of clinical symptoms, such as bloody stools, renal hemorrhage, hemoptysis, and pleural effusion during menstruation [2, 3]. However, the simultaneous occurrence of endometriosis and ascites is rather rare, being reported to occur only in 60 women up to date [8–64]. The pathogenesis of this rare pathology is still a matter of debate. Being the first to postulate a theory for the endometriosis-associated ascites, Bernstein et al. [12] have suggested that endometrial cells shed into the peritoneal cavity so that peritoneal cells are stimulated and ascites may eventually occur. Another hypothesis is that the rupture of endometriotic cysts results in irritation of peritoneal cells and subsequent formation of a reactive exudate. Also it has been proposed that ascites can be caused by hepatic involvement of cystic endometriosis [48, 49, 61]. The vast majority of the women presenting with endometriosis-related ascites were non-Caucasian and nulliparous women of reproductive age. The women diagnosed with endometriosis-related ascites usually complain of abdominal distention, abdominal or pelvic pain, and weight loss. Nevertheless, the symptoms of endometriosis, such as dysmenorrhea and menstrual exacerbation are revealed when they are questioned carefully [8–64]. The women who present with endometriosis-related ascites usually have advanced disease which involves fallopian tubes, ovaries, appendix, sigmoid colon, and omentum. Moreover, pelvic implants and extensive adhesions are



specified in 15.0% of the reviewed subjects [15, 18, 41, 47–50, 54, 62]. Due to the existence of widespread disease, there is a high risk of recurrence in women with endometriosisassociated ascites. Ascites arising in a woman with endometriosis usually demonstrates the characteristics of an exudate. This allows the acquirement of ascetic fluid through paracentesis so that endometriosis can be successfully detected by means of cytological examination. However, most of the patients presenting with endometriosis-related ascites were diagnosed after operative assessment and their diagnosis was confirmed by histological assessment [61, 62]. The definitive diagnosis of endometriosis-related ascites is usually made during operative assessment or after the exclusion of other clinical entities causing ascites. These clinical entities account for ovarian malignancy, liver disease, renal disease, cardiac disease, pancreatic disease, and tuberculosis [5–7]. The cytologic diagnosis of peritoneal endometriosis can be difficult because the acquired samples of ascetic fluid may reveal no particular cells except non-specific hemosiderin or hemofuscin-laden macrophages [31, 32, 36, 51]. Zeppa et al. [51] mentioned about the microscopic appearance of mesothelial cells and histiocytes on a hemorrhagic background in specimens derived from ascetic fluid. Also they observed the monomorphous small cells which had scanty cytoplasm and small nuclei with even smaller nucleoli and dispersed chromatin. Since these cells were tightly packed in a honeycomb pattern and organized in typical glove shape, they strongly resembled the cells located within the endometrial glands. On the other hand, histopathological assessment of peritoneal biopsies may be of more help as they would reveal slightly hyperplastic endometrial cells embedded within a dense stroma [32]. Ascites associated with endometriosis is mostly massive and may be concurrent with pleural effusion. Endometriosis-associated pleural effusion was also diagnosed in 40% of the reviewed subjects with endometriosis-related ascites [8, 9, 11, 12, 23, 29, 33–37, 39, 41, 45, 48, 50, 54–56, 62]. It has been hypothesized that menstrual debris may breech the diaphragm via fenestrations, or access the lymphatics, with subsequent seeding of the pleura or lung parenchyma. However, such an extensive involvement would only sometimes lead to the evasion of intravascular fluid into the extracellular compartment. Therefore, it can be proposed that it is the quantity of the seeded menstrual material and the individual inflammatory reaction which determine whether such a spread of menstrual material would result in clinical occurrence of ascites and/or pleural effusion [59–62]. A body of evidence for this assumption is that the clinical features of the women with endometriosis-related ascites and pleural effusion are similar to those of the


Arch Gynecol Obstet (2011) 283:513–518

women with only endometriosis-associated ascites. Thus, it can be assumed that the same pathophysiological mechanism is accountable for the occurrence of endometriosisrelated ascites and endometriosis-related ascites and pleural effusion [8–64]. Another clue may be the case report which describes the emergence of endometriosisassociated ascites in a woman with acquired immunodeficiency syndrome. It has been concluded that acquired immunodeficiency can trigger the progression of endometriosis so that massive ascites develops rapidly [60]. The management of endometriosis-related ascites is the same as that of endometriosis. Hence the cessation of ovarian functions either by surgery or by chemotherapy is required for the definitive treatment of ascites which is associated with endometriosis. Ovarian functions can be annihilated either by a progestational agent or by a gonadotropin releasing hormone (GnRH) agonist. Although GnRH agonists have been successfully used to manage endometriosis and its related diseases, medical castration is obviously less efficient than surgical castration and cannot prevent recurrence in some instances. That is why patients who receive medical treatment need long follow-up with suppression [8–64]. Another option is surgical treatment which can be done either conservatively or radically. The decision for the definitive surgical treatment can be made depending upon several factors, such as patient’s compliance with medical management, personal preference, severity of the disease, and the patient’s desire for fertility. Since estrogen alone may exacerbate the residual foci of endometriosis, patients who have undergone total abdominal hysterectomy and bilateral salpingo-oopherectomy should not be prescribed with unopposed estrogen. Patients who desire to preserve their fertility and opt for medical treatment may require in vitro fertilization because of extensive pelvic adhesions. It should be noted that such patients may develop ascites during ovulation induction. Thus, ovarian cryopreservation may present another choice [8–64]. Up to date, corticosteroid treatment, thoracentesis, and pleurectomy have been carried out to treat pleural effusion. Amongst these, thoracentesis seems to be the most efficient and convenient approach. However, the definitive treatment of endometriosis-related pleural effusion is the correction of underlying pathology [8, 9, 11, 12, 23, 29, 33–37, 39, 41, 45, 48, 50, 54–56, 62, 64]. In summary, endometriosis-associated ascites and/or pleural effusion usually refers to extensive disease which has a high risk for recurrence. Endometriosis presenting with ascites usually affects non-Caucasian nulliparous women of reproductive age and usually leads to clinical symptoms and elevated serum CA 125 concentrations so that suspicion of an ovarian malignancy arises. Whenever endometriosis-associated ascites is diagnosed, it should be investigated whether pleural effusion exists or not. Since

Arch Gynecol Obstet (2011) 283:513–518

clinical features of the women with endometriosis-related ascites and pleural effusion mostly resemble those of the women with endometriosis-related ascites, it can be assumed that the same pathophysiological mechanism is responsible for both clinical entities. Therefore, clinicians should consider endometriosis in differential diagnosis of pelvic masses and also include endometriosis in diagnostic workup of ascites or pleural effusion. Acknowledgments We acknowledge our colleagues for their help in the translation of non-English papers. Conflict of interest


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